Spliceosomal protein eftud2 mutation leads to p53-dependent apoptosis in zebrafish neural progenitors

Haploinsufficiency of EFTUD2 (Elongation Factor Tu GTP Binding Domain Containing 2) is linked to human mandibulofacial dysostosis, Guion-Almeida type (MFDGA), but the underlying cellular and molecular mechanisms remain to be addressed. We report here the isolation, cloning and functional analysis of...

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Published in:Nucleic acids research Vol. 45; no. 6; pp. 3422 - 3436
Main Authors: Lei, Lei, Yan, Shou-Yu, Yang, Ran, Chen, Jia-Yu, Li, Yumei, Bu, Ye, Chang, Nannan, Zhou, Qinchao, Zhu, Xiaojun, Li, Chuan-Yun, Xiong, Jing-Wei
Format: Journal Article
Language:English
Published: England Oxford University Press 07.04.2017
Subjects:
Animals
Apoptosis
Brain - abnormalities
Cloning, Molecular
Exons
Introns
Mutation
Neural Stem Cells - cytology
Neurogenesis - genetics
Neurons - cytology
Nonsense Mediated mRNA Decay
Peptide Elongation Factors - genetics
RNA
RNA Splicing
RNA Splicing Factors - genetics
Spinal Cord - abnormalities
Transcriptome
Tumor Suppressor Protein p53 - metabolism
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish Proteins - genetics
Zebrafish Proteins - metabolism
ISSN:0305-1048, 1362-4962
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Abstract Haploinsufficiency of EFTUD2 (Elongation Factor Tu GTP Binding Domain Containing 2) is linked to human mandibulofacial dysostosis, Guion-Almeida type (MFDGA), but the underlying cellular and molecular mechanisms remain to be addressed. We report here the isolation, cloning and functional analysis of the mutated eftud2 (snu114) in a novel neuronal mutant fn10a in zebrafish. This mutant displayed abnormal brain development with evident neuronal apoptosis while the development of other organs appeared less affected. Positional cloning revealed a nonsense mutation such that the mutant eftud2 mRNA encoded a truncated Eftud2 protein and was subjected to nonsense-mediated decay. Disruption of eftud2 led to increased apoptosis and mitosis of neural progenitors while it had little effect on differentiated neurons. Further RNA-seq and functional analyses revealed a transcriptome-wide RNA splicing deficiency and a large amount of intron-retaining and exon-skipping transcripts, which resulted in inadequate nonsense-mediated RNA decay and activation of the p53 pathway in fn10a mutants. Therefore, our study has established that eftud2 functions in RNA splicing during neural development and provides a suitable zebrafish model for studying the molecular pathology of the neurological disease MFDGA.
AbstractList Haploinsufficiency of EFTUD2 (Elongation Factor Tu GTP Binding Domain Containing 2) is linked to human mandibulofacial dysostosis, Guion-Almeida type (MFDGA), but the underlying cellular and molecular mechanisms remain to be addressed. We report here the isolation, cloning and functional analysis of the mutated eftud2 (snu114) in a novel neuronal mutant fn10a in zebrafish. This mutant displayed abnormal brain development with evident neuronal apoptosis while the development of other organs appeared less affected. Positional cloning revealed a nonsense mutation such that the mutant eftud2 mRNA encoded a truncated Eftud2 protein and was subjected to nonsense-mediated decay. Disruption of eftud2 led to increased apoptosis and mitosis of neural progenitors while it had little effect on differentiated neurons. Further RNA-seq and functional analyses revealed a transcriptome-wide RNA splicing deficiency and a large amount of intron-retaining and exon-skipping transcripts, which resulted in inadequate nonsense-mediated RNA decay and activation of the p53 pathway in fn10a mutants. Therefore, our study has established that eftud2 functions in RNA splicing during neural development and provides a suitable zebrafish model for studying the molecular pathology of the neurological disease MFDGA.
Author Zhou, Qinchao
Li, Yumei
Yang, Ran
Yan, Shou-Yu
Li, Chuan-Yun
Xiong, Jing-Wei
Bu, Ye
Chen, Jia-Yu
Lei, Lei
Zhu, Xiaojun
Chang, Nannan
AuthorAffiliation Institute of Molecular Medicine, Beijing Key Laboratory of Cardiometabolic Molecular Medicine, and State Key Laboratory of Natural and Biomimetic Drugs, Peking University, Beijing 100871, China
AuthorAffiliation_xml – name: Institute of Molecular Medicine, Beijing Key Laboratory of Cardiometabolic Molecular Medicine, and State Key Laboratory of Natural and Biomimetic Drugs, Peking University, Beijing 100871, China
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SSID ssj0014154
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Snippet Haploinsufficiency of EFTUD2 (Elongation Factor Tu GTP Binding Domain Containing 2) is linked to human mandibulofacial dysostosis, Guion-Almeida type (MFDGA),...
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StartPage 3422
SubjectTerms Animals
Apoptosis
Brain - abnormalities
Cloning, Molecular
Exons
Introns
Mutation
Neural Stem Cells - cytology
Neurogenesis - genetics
Neurons - cytology
Nonsense Mediated mRNA Decay
Peptide Elongation Factors - genetics
RNA
RNA Splicing
RNA Splicing Factors - genetics
Spinal Cord - abnormalities
Transcriptome
Tumor Suppressor Protein p53 - metabolism
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish Proteins - genetics
Zebrafish Proteins - metabolism
Title Spliceosomal protein eftud2 mutation leads to p53-dependent apoptosis in zebrafish neural progenitors
URI https://www.ncbi.nlm.nih.gov/pubmed/27899647
https://www.proquest.com/docview/1845247881
https://pubmed.ncbi.nlm.nih.gov/PMC5389467
Volume 45
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